Skip to main content
SpringerLink
Log in

Heterologous expression of kiwifruit (Actinidia chinensis) GOLDEN2-LIKE homolog elevates chloroplast level and nutritional quality in tomato (Solanum lycopersicum)

  • Original Article
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

Constitutive expression of AchGLK from A. chinensis in transgenic tomato (S. lycopersicum) confers fruits an elevated plastid biogenesis with intensified granule thylakoid stacks and increased content of nutritional compounds.

Plastid development is regulated by multiple environmental and genetic factors. Golden2-like (GLK) genes, members from GARP subfamily of the MYB transcription factors, have been shown to regulate plastid biogenesis and development in several species. In tomato (S. lycopersicum), SlGLK2 gene is expressed in the fruit in a manner of latitudinal gradient and determines the green shoulder phenotype. Here, we report the isolation and characterization of a kiwifruit (A. chinensis) GLK homolog (AchGLK). Transcription analysis showed that AchGLK is highly expressed in mature leaves and in fruits 60-day post-anthesis. Overexpression of AchGLK in transgenic tomato resulted in dark green immature fruit with higher concentration of chlorophyll and overall increased chloroplast compartment, both number and size. The ripened fruit had higher levels of carotenoids and sugars as well. Nevertheless, no phenotypic changes were observed in the transgenic leaves, similar to the previously described overexpression of SlGLK2 in tomato. Our study suggests that AchGLK is functionally homologous to tomato GLK2 with a potential in regulating plastid level in fruit that could contribute to improvement of fruit quality.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6

Similar content being viewed by others

Abbreviations

DPA:

Day post-anthesis

GLK:

GOLDEN2-LIKE

NLS:

Nuclear localization signal

References

  • Al Khateeb WM, Schroeder DF (2007) DDB2, DDB1A and DET1 exhibit complex interactions during Arabidopsis development. Genetics 176:231–242

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ampomah-Dwamena C, McGhie T, Wibisono R, Montefiori M, Hellens RP, Allan AC (2009) The kiwifruit lycopene beta-cyclase plays a significant role in carotenoid accumulation in fruit. J Exp Bot 60(13):3765–3779

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baldwin EA, Goodner K, Plotto A (2008) Interaction of volatiles sugars, and acids on perception of tomato aroma and flavor descriptors. J Food Sci 73(6):S294–S307

    Article  CAS  PubMed  Google Scholar 

  • Bernhardt A, Lechner E, Hano P, Schade V, Dieterie M, Anders M, Dubin MJ, Benvenuto G, Bowler C, Genschik P, Hellmann H (2006) CUL4 associates with DDB1 and DET1 and its downregulation affects diverse aspects of development in Arabidopsis thaliana. Plant J 47(4):591–603

    Article  CAS  PubMed  Google Scholar 

  • Bino RJ, Ric De Vos CH, Lieberman M, Hall RD, Bovy A, Jonker HH, Tikunov Y, Lommen A, Moco S, Levin I (2005) The light-hyperresponsive high pigment-2dg mutation of tomato: alterations in the fruit metabolome. New Phytol 166(2):427–438

    Article  CAS  PubMed  Google Scholar 

  • Bravo-Garcia A, Yasumura Y, Langdale JA (2009) Specialization of the Golden2-like regulatory pathway during land plant evolution. New Phytol 183(1):133–141

    Article  CAS  PubMed  Google Scholar 

  • Butler L (1952) The linkage map of the tomato. J Hered 43:25

    Article  Google Scholar 

  • Chen H, Shen Y, Tang X, Yu L, Wang J, Guo L, Zhang Y, Zhang H, Feng S, Strickland E, Zheng N, Deng XW (2006) Arabidopsis CULLIN4 forms an E3 ubiquitin ligase with RBX1 and the CDD complex in mediating light control of development. Plant Cell 18(8):1991–2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Davuluri GR, van Tuinen A, Fraser PD, Manfredonia A, Newman R, Burgess D, Brummell DA, King SR, Palys J, Uhlig J, Bramley PM, Pennings HM, Bowler C (2005) Fruit-specific RNAi-mediated suppression of DET1 enhances carotenoid and flavonoid content in tomatoes. Nat Biotechnol 23(7):890–895

    Article  CAS  PubMed  Google Scholar 

  • Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinf 5:113

    Article  Google Scholar 

  • Fillatti JJ, Kiser J, Rose R, Comai L (1987) Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector. Nat Biotechnol 5:726–730

    Article  CAS  Google Scholar 

  • Finn RD, Bateman A, Clements J, Coggill P, Eberhardt RY, Eddy SR, Sonnhammer EL, Bateman A (2014) Pfam: the protein families database. Nucleic Acids Res 42:D222–D230

    Article  CAS  PubMed  Google Scholar 

  • Fitter DW, Martin DJ, Copley MJ, Scotland RW, Langdale JA (2002) GLK gene pairs regulate chloroplast development in diverse plant species. Plant J 31(6):713–727

    Article  CAS  PubMed  Google Scholar 

  • Galpaz N, Wang Q, Menda N, Zamir D, Hirschberg J (2008) Abscisic acid deficiency in the tomato mutant high-pigment 3 leading to increased plastid number and higher fruit lycopene content. Plant J 53:717–730

    Article  CAS  PubMed  Google Scholar 

  • Hetherington SE, Smillie RM, Davies WJ (1998) Photosynthetic activities of vegetative and fruiting tissues of tomato. J Exp Bot 49(324):1173–1181

    Article  CAS  Google Scholar 

  • Huang S, Ding J, Deng D, Tang W, Sun H et al (2013) Draft genome of the kiwifruit Actinidia chinensis. Nat Commun 4:2640

    PubMed  PubMed Central  Google Scholar 

  • Kendrick RE, Peters JL, Kerckhoffs LH, van Tuinen A, Koornneef M (1994) Photomorphogenic mutants of tomato. Biochem Soc Symp 60:249–256

    CAS  PubMed  Google Scholar 

  • Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45:41–59

    Article  CAS  PubMed  Google Scholar 

  • Klee H, Tieman D (2002) The tomato ethylene receptor gene family: form and function. Physiol Plant 115(3):336–341

    Article  CAS  PubMed  Google Scholar 

  • Kobayashi K, Baba S, Obayashi T, Sato M, Toyooka K, Keranen M, Aro EM, Fukaki H, Ohta H, Sugimoto K, Masuda T (2012) Regulation of root greening by light and auxin/cytokinin signaling in Arabidopsis. Plant Cell 24:1081–1095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kolotilin I, Koltai H, Tadmor Y, Bar-Or C, Reuveni M, Meir A, Nahon S, Shlomo H, Chen L, Levin I (2007) Transcriptional profiling of high pigment-2dg tomato mutant links early fruit plastid biogenesis with its overproduction of phytonutrients. Plant Physiol 145(2):389–401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kosugi S, Hasebe M, Tomita M, Yanagawa H (2009) Systematic identification of cell cycle-dependent yeast nucleocytoplasmic shuttling proteins by prediction of composite motifs. Proc Natl Acad Sci USA 106(25):10171–10176

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kumar S, Stecher G, Tamura K (2016) MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol Biol Evol 33(7):1870–1874

    Article  CAS  PubMed  Google Scholar 

  • Laing WA, Bulley S, Wright M, Cooney J, Jensen D, Barraclough D, MacRae E (2004) A highly specific L-galactose-1-phosphate phosphatase on the path to ascorbate biosynthesis. Proc Natl Acad Sci USA 101:16976–16981

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Laing WA, Wright MA, Cooney J, Bulley SM (2007) The missing step of the L-galactose pathway of ascorbate biosynthesis in plants, an l-galactose guanyltransferase, increases leaf ascorbate content. Proc Natl Acad Sci USA 104:9534–9539

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lavi N, Tadmor Y, Meir A, Bechar A, Oren-shamir M, Ovadia R, Reuveni M, Nahon S, Shlomo H, Chen L, Levin I (2009) Characterization of the INTENSE PIGMENT tomato genotype emphasizing targeted fruit metabolites and chloroplast biogenesis. J Agric Food Chem 57(11):4818–4826

    Article  CAS  PubMed  Google Scholar 

  • Ledger SE, Janssen BJ, Karunairetnam S, Wang T, Snowden KC (2010) Modified CAROTENOID CLEAVAGE DIOXYGENASE8 expression correlates with altered branching in kiwifruit (Actinidia chinensis). New Phytol 188:803–813

    Article  CAS  PubMed  Google Scholar 

  • Li Y, Deng H, Miao M, Li H, Huang S, Wang S, Liu Y (2016) Tomato MBD5, a methyl CpG binding domain protein, physically interacting with UV-damaged DNA binding protein-1, functions in multiple process. New Phytol 210(1):208–226

    Article  CAS  PubMed  Google Scholar 

  • Lieberman M, Segev O, Gilboa N, Lalazar A, Levin I (2004) The tomato homolog of the gene encoding UV-damaged DNA binding protein 1 (DDB1) underlined as the gene that causes the high pigment-1 mutant phenotype. Theor Appl Genet 108:1574–1581

    Article  CAS  PubMed  Google Scholar 

  • Liu Y, Roof S, Ye Z, Barry C, van Tuinen A, Vrebalov J, Bowler C, Giovannoni J (2004) Manipulation of light signal transduction as a means of modifying fruit nutritional quality in tomato. Proc Natl Acad Sci USA 101(26):9897–9902

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lopez-Juez E, Pyke KA (2005) Plastids unleashed: their development and their integration in plant development. Int J Dev Biol 49:557–577

    Article  CAS  PubMed  Google Scholar 

  • Ma C, Sun Z, Chen C, Zhang L, Zhu S (2014) Simultaneous separation and determination of fructose, sorbitol, glucose and sucrose in fruits by HPLC-ELSD. Food Chem 145:784–788

    Article  CAS  PubMed  Google Scholar 

  • Molinier J, Lechner E, Dumbliauskas E, Genschik P (2008) Regulation and role of Arabidopsis CUL4-DDB1A-DDB2 in maintaining genome integrity upon UV stress. PLoS Genet 4(6):e1000093

    Article  PubMed  PubMed Central  Google Scholar 

  • Montefiori M, Espley RV, Stevenson D, Cooney J, Datson PM, Saiz A, Atkinson RG, Hellens RP, Allan AC (2011) Identification and characterisation of F3GT1 and F3GGT1, two glycosyltransferases responsible for anthocyanin biosynthesis in red-fleshed kiwifruit (Actinidia chinensis). Plant J 65:106–118

    Article  CAS  PubMed  Google Scholar 

  • Mustilli AC, Fenzi F, Ciliento R, Alfano F, Bowler C (1999) Phenotype of the tomato high pigment-2 mutant is caused by a mutation in the tomato homolog of DEETIOLATED1. Plant Cell 11(2):145–157

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nakamura H, Muramatsu M, Hakata M, Ueno O, Nagamura Y, Hirochika H, Takano M, Ichikawa H (2009) Ectopic overexpression of the transcription factor OsGLK1 induces chloroplast development in non-green rice cells. Plant Cell Physiol 50(11):1933–1949

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nashilevitz S, Melamed-Bessudo C, Izkovich Y, Rogachev I, Osorio S, Itkin M, Adato A, Pankratov I, Hirchberg J, Fernie AR, Wolf S, Usadel B, Levy AA, Rumeau D, Aharoni A (2010) An Orange Ripening mutant links plastid NAD(P)H dehydrogenase complex activity to central and specialized metabolism during tomato fruit maturation. Plant Cell 22(6):1977–1997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nguyen CV, Vrebalov JT, Gapper NE, Zheng Y, Zhong S, Fei Z, Giovannoni JJ (2014) Tomato GOLDEN2-LIKE transcription factors reveal molecular gradients that function during fruit development and ripening. Plant Cell 26(2):585–601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Osteryoung KW, Pyke KA (2014) Division and dynamic morphology of plastids. Annu Rev Plant Biol 65:443–472

    Article  CAS  PubMed  Google Scholar 

  • Park YS, Im MH, Ham KS, Kang SG, Park YK, Namiesnik J, Leontowicz H, Leontowicz M, Katrich E, Gorinstein S (2013) Nutritional and pharmaceutical properties of bioactive compounds in organic and conventional growing kiwifruit. Plant Foods Hum Nutr 68:57–64

    Article  CAS  PubMed  Google Scholar 

  • Petriccione M, Mastrobuoni F, Zampella L, Scortichini M (2015) Reference gene selection for normalization of RT-qPCR gene expression data from Actinidia deliciosa leaves infected with Pseudomonas syringae pv. actinidiae. Sci Rep 5:16961

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Piechulla B, Glick R, Bahl H, Melis A, Gruissem W (1987) Changes in photosynthetic capacity and photosynthetic protein pattern during tomato fruit ripening. Plant Physiol 84(3):911–917

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pilkington SM, Montefiori M, Jameson PE, Allan AC (2012) The control of chlorophyll levels in maturing kiwifruit. Planta 236:1615–1628

    Article  CAS  PubMed  Google Scholar 

  • Pogson BJ, Woo NS, Forster B, Small ID (2008) Plastid signaling to the nucleus and beyond. Trends Plant Sci 13:602–609

    Article  CAS  PubMed  Google Scholar 

  • Powell ALT, Nguyen CV, Hill T, Cheng KL, Figueroa-Balderas R, Aktas H, Ashrafi H, Pons C, Fernandez-Munoz R, Lopez-Baltazar J, Barry CS, Liu Y, Chetelat R, Granell A, Van Deynze A, Giovannoni JJ, Bennett AB (2012) Uniform ripening encodes a Golden 2-like transcription factor regulating tomato fruit chloroplast development. Science 336(6089):1711–1715

    Article  CAS  PubMed  Google Scholar 

  • Ronen G, Carmel-Goren L, Zamir D, Hirschberg J (2000) An alternative pathway to beta-carotene formation in plant chromoplasts discovered by map-based cloning of beta and old-gold color mutations in tomato. Proc Natl Acad Sci USA 97(20):11102–11107

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rossini L, Cribb L, Martin DJ, Langdale JA (2001) The maize Golden2 gene defines a novel class of transcriptional regulators in plants. Plant Cell 13(5):1231–1244

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sagar M, Chervin C, Mila I, Hao Y, Roustan JP, Benichou M, Gibon Y, Biais B, Maury P, Latche A, Pech JC, Bouzayen M, Zouine M (2013) SlARF4, an anxin response factor involved in the control of sugar metabolism during tomato fruit development. Plant Physiol 161:1362–1374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sambrook J, Russell D (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York

    Google Scholar 

  • Tang X, Tang Z, Huang S, Liu J, Liu J, Shi W, Tian X, Li Y, Zhang D, Yang J, Gao Y, Zeng D, Hou P, Niu X, Cao Y, Li G, Li X, Xiao F, Liu Y (2013) Whole transcriptome sequencing reveals genes involved in plastid/chloroplast division and development are regulated by the HP1/DDB1 at an early stage of tomato fruit development. Planta 238(5):923–936

    Article  CAS  PubMed  Google Scholar 

  • Tang W, Zheng Y, Dong J, Yu J, Yue J, Liu F, Guo X, Huang S, Wisniewski M, Sun J, Niu X, Ding J, Liu J, Fei Z, Liu Y (2016a) Comprehensive transcriptome profiling reveals long noncoding RNA expression and alternative splicing regulation during fruit development and ripening in kiwifruit (Actinidia chinensis). Front Plant Sci 7:335

    PubMed  PubMed Central  Google Scholar 

  • Tang X, Miao M, Niu X, Zhang D, Cao X, Jin X, Zhu Y, Fan Y, Wang H, Liu Y, Sui Y, Wang W, Wang A, Xiao F, Giovannoni J, Liu Y (2016b) Ubiquitin-conjugated degradation of golden 2-like transcription factor is mediated by CUL4-DDB1-based E3 ligase complex in tomato. New Phytol 209(3):1028–1039

    Article  CAS  PubMed  Google Scholar 

  • Wang S, Liu J, Feng Y, Niu X, Giovannoni J, Liu Y (2008) Altered plastid levels and potential for improved fruit nutrient content by downregulation of the tomato DDB1-interacting protein CUL4. Plant J 55:89–103

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Fouracre J, Kelly S, Karki S, Gowik U, Aubry S, Shaw MK, Westhoff P, Slamet-Loedin IH, Quick WP, Hibberd JM, Langdale JA (2013) Evolution of GOLDEN2-LIKE gene function in C3 and C4 plants. Planta 237:481–495

    Article  CAS  PubMed  Google Scholar 

  • Wang P, Khoshravesh R, Karki S, Tapia R, Balahadia CP, Bandyopadhyay A, Quick WP, Furbank R, Sage TL, Langdale JA (2017) Re-creation of a key step in the evolutionary switch from C3 to C4 leaf anatomy. Curr Biol 27(21):3278–3287

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Waters MT, Wang P, Korkaric M, Capper RG, Saunders NJ, Langdale JA (2009) GLK transcription factors coordinate expression of the photosynthetic apparatus in Arabidopsis. Plant Cell 21:1109–1128

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wertz IE, O’Rourke KM, Zhang Z, Dornan D, Arnott D, Deshaies RJ, Dixit VM (2004) Human De-etiolated-1 regulates c-Jun by assembling a CUL4A ubiquitin ligase. Science 303(5662):1371–1374

    Article  CAS  PubMed  Google Scholar 

  • Yasumura Y, Moylan EC, Langdale JA (2005) A conserved transcription factor mediates nuclear control of organelle biogenesis in anciently diverged land plants. Plant Cell 17:1894–1907

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yue J, Liu J, Ban R, Tang W, Deng L, Fei Z, Liu Y (2015) Kiwifruit information resource (KIR): a comparative platform for kiwifruit genomics. Database 2015:bav113

    Article  PubMed  PubMed Central  Google Scholar 

  • Zuo LL, Wang ZY, Fan ZL, Tian SQ, Liu JR (2012) Evaluation of antioxidant and antiproliferative properties of three Actinidia (Actinidia kolomikta, Actinidia arguta, Actinidia chinensis) extracts in vitro. Int J Mol Sci 13:5506–5518

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work has been financially supported by the National Natural Science Foundation of China (31701922, 31671259, 31461143008, and 31471157), and the Fundamental Research Funds for the Central Universities (113-4115104003 and 113-4115104004).

Author information

Author notes

  1. Guangwei Li and Danyang Chen contributed equally to this article.

Authors and Affiliations

  1. School of Biotechnology and Food Engineering, Hefei University of Technology, Hefei, 230009, China

    Guangwei Li, Danyang Chen, Xiaofeng Tang & Yongsheng Liu

  2. Ministry of Education Key Laboratory for Bio-resource and Eco-environment, College of Life Science, State Key Laboratory of Hydraulics and Mountain River Engineering, Sichuan University, Chengdu, 610064, China

    Yongsheng Liu

Authors
  1. Guangwei Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Danyang Chen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Xiaofeng Tang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Yongsheng Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Xiaofeng Tang or Yongsheng Liu.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Li, G., Chen, D., Tang, X. et al. Heterologous expression of kiwifruit (Actinidia chinensis) GOLDEN2-LIKE homolog elevates chloroplast level and nutritional quality in tomato (Solanum lycopersicum). Planta 247, 1351–1362 (2018). https://doi.org/10.1007/s00425-018-2853-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-018-2853-6

Keywords

Search

Navigation